Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs

Host organisms are believed to evolve defense mechanisms (i.e., resistance and/or tolerance) under selective pressures exerted by natural enemies. A prerequisite for the evolution of resistance and tolerance is the existence of genetic variation in these traits for natural selection to act. However, selection for resistance and/or tolerance may be constrained by negative genetic correlations with other traits that affect host fitness. We studied genetic variation in resistance and tolerance against parasitic infection and the potential fitness costs associated with these traits using a novel study system, namely the interaction between a flowering plant and a parasitic plant. In this system, parasitic infection has significant negative effects on host growth and reproduction and may thus act as a selective agent. We conducted a greenhouse experiment in which we grew host plants, Urtica dioica, that originated from a single natural population and represented 20 maternal families either uninfected or infected with the holoparasitic dodder, Cuscuta europaea. that originated from the same site. We calculated correlations among resistance, tolerance, and host performance to test for costs of resistance and tolerance. We measured resistance as parasite performance (quantitative resistance) and tolerance as the slopes of regressions relating the vegetative and reproductive biomass of host plants to damage level (measured as parasite biomass). We observed significant differences among host families in parasite resistance and in parasite tolerance in terms of reproductive biomass, a result that suggests genetic variation in these traits. Furthermore, we found differences in resistance and tolerance between female and male host plants. In addition, the correlations indicate costs of resistance in terms of host growth and reproduction and costs of tolerance in terms of host reproduction. Our results thus indicate that host tolerance and resistance can evolve as a response to infection by a parasitic plant and that costs of resistance and tolerance may be one factor maintaining genetic variation in these traits.     

Male field crickets that provide reproductive benefits to females incur higher costs

Abstract.  1. Females often select mates based on signals correlated with the quality of the direct benefits that males will provide to them. A male's quality as a mate and the structure of his mating signals may covary because both traits are energetically expensive for males to produce and because both traits are affected by short-term changes in nutritional condition.
2. In the variable field cricket, Gryllus lineaticeps , previous work has shown that females receive reproductive benefits from males that produce higher chirp rates and lifespan benefits from males that produce longer chirp durations, even when they only receive the sperm and seminal fluid contained in male spermatophores. Higher chirp rates are energetically expensive for males to produce, and chirp rate is strongly affected by diet quality, whereas longer chirp durations do not appear to be expensive for males to produce, and chirp duration does not appear to be affected by male diet quality. In this study two hypotheses were tested about the energetic costs of spermatophore production: (1) that spermatophores are expensive for males to produce and (2) that males providing greater direct benefits to females incur higher costs of spermatophore production.
3. Males that were provided with a lower quality diet took longer to produce a new spermatophore. This result suggests that spermatophores are costly for males to produce.
4. Males that produced higher chirp rates took longer to produce a new spermatophore. This result suggests that male chirp rate and female reproductive benefits may covary because both traits are energetically expensive for males to produce and thus are affected by male nutritional condition. There was no association, however, between male chirp duration and spermatophore production time.     

Sperm competition and brain size evolution in mammals

The ‘expensive tissue hypothesis’ predicts a size trade‐off between the brain and other energetically costly organs. A specific version of this hypothesis, the ‘expensive sexual tissue hypothesis’, argues that selection for larger testes under sperm competition constrains brain size evolution. We show here that there is no general evolutionary trade‐off between brain and testis mass in mammals. The predicted negative relationship between these traits is not found for rodents, ungulates, primates, carnivores, or across combined mammalian orders, and neither does total brain mass vary according to the level of sperm competition as determined by mating system classifications. Although we are able to confirm previous reports of a negative relationship between brain and testis mass in echolocating bats, our results suggest that mating system may be a better predictor of brain size in this group. We conclude that the expensive sexual tissue hypothesis accounts for little or none of the variance in brain size in mammals, and suggest that a broader framework is required to understand the costs of brain size evolution and how these are met.     

Does investment into ��expensive�� tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts

Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in ??expensive?? tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.     

Influence of Developmental Conditions on Immune Function and Dispersal-Related Traits in the Glanville Fritillary (Melitaea cinxia) Butterfly

Organisms in the wild are constantly faced with a wide range of environmental variability, such as fluctuation in food availability. Poor nutritional conditions influence life-histories via individual resource allocation patterns, and trade-offs between competing traits. In this study, we assessed the influence of food restriction during development on the energetically expensive traits flight metabolic rate (proxy of dispersal ability), encapsulation rate (proxy of immune defence), and lifespan using the Glanville fritillary butterfly, Melitaea cinxia, as a model organism. Additionally, we examined the direct costs of flight on individual immune function, and whether those costs increase under restricted environmental conditions. We found that nutritional restriction during development enhanced adult encapsulations rate, but reduced both resting and flight metabolic rates. However, at the individual level metabolic rates were not associated with encapsulation rate. Interestingly, individuals that were forced to fly prior to the immune assays had higher encapsulation rates than individuals that had not flown, suggesting that flying itself enhances immune response. Finally, in the control group encapsulation rate correlated positively with lifespan, whereas in the nutritional restriction group there was no relationship between these traits, suggesting that the association between encapsulation rate on adult lifespan was condition-dependent. Thus stressful events during both larval development (food limitation) and adulthood (forced flight) induce increased immune response in the adult butterflies, which may allow individuals to cope with stressful events later on in life.     

A MULTIVARIATE ANALYSIS OF GENETIC VARIATION IN THE ADVERTISEMENT CALL OF THE GRAY TREEFROG,HYLA VERSICOLOR

Genetic variation in sexual displays is crucial for an evolutionary response to sexual selection, but can be eroded by strong selection. Identifying the magnitude and sources of additive genetic variance underlying sexually selected traits is thus an important issue in evolutionary biology. We conducted a quantitative genetics experiment with gray treefrogs (Hyla versicolor) to investigate genetic variances and covariances among features of the male advertisement call. Two energetically expensive traits showed significant genetic variation: call duration, expressed as number of pulses per call, and call rate, represented by its inverse, call period. These two properties also showed significant genetic covariance, consistent with an energetic constraint to call production. Combining the genetic variance–covariance matrix with previous estimates of directional sexual selection imposed by female preferences predicts a limited increase in call duration but no change in call rate despite significant selection on both traits. In addition to constraints imposed by the genetic covariance structure, an evolutionary response to sexual selection may also be limited by high energetic costs of long‐duration calls and by preferences that act most strongly against very short‐duration calls. Meanwhile, the persistence of these preferences could be explained by costs of mating with males with especially unattractive calls.     

Are secondary sex traits, parasites and immunity related to variation in primary sex traits in the Arctic charr?

Primary and secondary sex traits are influenced by the same sex hormones, and the expression of secondary sex traits may consequently signal males' capacity for sperm production. Sperm quality may also be influenced by immune activity, as sperm are non-self to the male. Parasite infections alter immune activity and may thus reduce ejaculate quality. In the Arctic charr (Salvelinus alpinus) the red abdominal colour is considered an ornament that signals important information in mate choice. We captured and individually caged sexually mature male Arctic charr during the spawning period. Afterwards we estimated abdominal colour, parasite infections, gonad mass and several spermatological and immunological variables. Intensity of abdominal colour was positively correlated to testes mass, milt mass and sperm cell numbers produced. Additionally, males with low parasite intensities had high testes mass and produced milt with high sperm density, indicating a trade-off between parasite resistance and development of primary sex traits. Our measures of immunity were, however, not related to primary sex traits. We conclude that females evaluating male abdominal coloration may obtain information about differences between males in fertilization potential and parasite resistance.     

Use of trade-off theory to advance understanding of herbivore–parasite interactions

• 1 Trade‐off theory has been extensively used to further our understanding of animal behaviour. In mammalian herbivores, it has been used to advance our understanding of their reproductive, parental care and foraging strategies. Here, we detail how trade‐off theory can be applied to herbivore–parasite interactions, especially in foraging environments.
• 2 Foraging is a common mode of uptake of parasites that represent the most pervasive challenge to mammalian fitness and survival. Hosts are hypothesized to alter their foraging behaviour in the presence of parasites in three ways: (i) hosts avoid foraging in areas that are contaminated with parasites; (ii) hosts select diets that increase their resistance and resilience to parasites; and (iii) hosts select for foods with direct anti‐parasitic properties (self‐medication). We concentrate on the mammalian herbivore literature to detail the recent advances made using trade‐off frameworks to understand the mechanisms behind host–parasite interactions in relation to these three hypotheses.
• 3 In natural systems, animals often face complex foraging decisions including nutrient intake vs. predation risk, nutrient intake vs. sheltering and nutrient intake vs. parasite risk trade‐offs. A trade‐off framework is detailed that can be used to interpret mammal behaviour in complex environments, and may be used to advance the self‐medication hypothesis.
• 4 The use of trade‐off theory has advanced our understanding of the contact process between grazing mammalian hosts and their parasites transmitted via the faecal–oral route. Experimental manipulation of the costs and benefits of a nutrient intake vs. parasite risk trade‐off has shown that environmental conditions (forage quality and quantity) and the physiological state (parasitic and immune status) of a mammalian host can both affect the behavioural decisions of foraging animals.
• 5 Naturally occurring trade‐offs and the potential to manipulate their costs and benefits enables us to identify the abilities and behavioural rules used by mammals when making decisions in complex environments and thus predict animal behaviour.

     

The target of selection matters: An established resistance—development‐time negative genetic trade‐off is not found when selecting on development time

Trade‐offs are fundamental to evolutionary outcomes and play a central role in eco‐evolutionary theory. They are often examined by experimentally selecting on one life‐history trait and looking for negative correlations in other traits. For example, populations of the moth Plodia interpunctella selected to resist viral infection show a life‐history cost with longer development times. However, we rarely examine whether the detection of such negative genetic correlations depends on the trait on which we select. Here, we examine a well‐characterized negative genotypic trade‐off between development time and resistance to viral infection in the moth Plodia interpunctella and test whether selection on a phenotype known to be a cost of resistance (longer development time) leads to the predicted correlated increase in resistance. If there is tight pleiotropic relationship between genes that determine development time and resistance underpinning this trade‐off, we might expect increased resistance when we select on longer development time. However, we show that selecting for longer development time in this system selects for reduced resistance when compared to selection for shorter development time. This shows how phenotypes typically characterized by a trade‐off can deviate from that trade‐off relationship, and suggests little genetic linkage between the genes governing viral resistance and those that determine response to selection on the key life‐history trait. Our results are important for both selection strategies in applied biological systems and for evolutionary modelling of host–parasite interactions.     

Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Host-parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency-dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype-by-genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all-resistant (or all-infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life-history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross-infection experiment showed significant host clone-by-parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.     

Vertebrate defense against parasites: Interactions between avoidance,resistance, and tolerance

Hosts can utilize different types of defense against the effects of parasitism, including avoidance, resistance, and tolerance. Typically, there is tremendous heterogeneity among hosts in these defense mechanisms that may be rooted in the costs associated with defense and lead to trade‐offs with other life‐history traits. Trade‐offs may also exist between the defense mechanisms, but the relationships between avoidance, resistance, and tolerance have rarely been studied. Here, we assessed these three defense traits under common garden conditions in a natural host–parasite system, the trematode eye‐fluke Diplostomum pseudospathaceum and its second intermediate fish host. We looked at host individuals originating from four genetically distinct populations of two closely related salmonid species (Atlantic salmon, Salmo salar and sea trout, Salmo trutta trutta) to estimate the magnitude of variation in these defense traits and the relationships among them. We show species‐specific variation in resistance and tolerance and population‐specific variation in resistance. Further, we demonstrate evidence for a trade‐off between resistance and tolerance. Our results suggest that the variation in host defense can at least partly result from a compromise between different interacting defense traits, the relative importance of which is likely to be shaped by environmental components. Overall, this study emphasizes the importance of considering different components of the host defense system when making predictions on the outcome of host–parasite interactions.     

Fitness outcomes in relation to individual variation in constitutive innate immune function

Although crucial for host survival when facing persistent parasite pressure, costly immune functions will inevitably compete for resources with other energetically expensive traits such as reproduction. Optimizing, but not necessarily maximizing, immune function might therefore provide net benefit to overall host fitness. Evidence for associations between fitness and immune function is relatively rare, limiting our potential to understand ultimate fitness costs of immune investment. Here, we assess how measures of constitutive immune function (haptoglobin, natural antibodies, complement activity) relate to subsequent fitness outcomes (survival, reproductive success, dominance acquisition) in a wild passerine (Malurus coronatus). Surprisingly, survival probability was not positively linearly predicted by any immune index. Instead, both low and high values of complement activity (quadratic effect) were associated with higher survival, suggesting that different immune investment strategies might reflect a dynamic disease environment. Positive linear relationships between immune indices and reproductive success suggest that individual heterogeneity overrides potential resource reallocation trade-offs within individuals. Controlling for body condition (size-adjusted body mass) and chronic stress (heterophil-lymphocyte ratio) did not alter our findings in a sample subset with available data. Overall, our results suggest that constitutive immune components have limited net costs for fitness and that variation in immune maintenance relates to individual differences more closely.     

Juvenile immune status affects the expression of a sexually selected trait in field crickets

Parasite-mediated sexual selection theory presumes that variation in sexual traits reliably reflects variation in parasite resistance among available mates. One mechanism that may warrant signal honesty involves costs of immune system activation in the case of a parasitic infection. We investigated this hypothesis in male field crickets Gryllus campestris, whose attractiveness to females depends on characteristics of the sound-producing harp that are essentially fixed following adult eclosion. During the nymphal stage, males subjected to one of two feeding regimes were challenged with bacterial lipopolysaccharides (LPS) to investigate condition-dependent effects on harp development as compared to other adult traits. Nymphal nutritional status positively affected adult body size, condition, and harp size. However, nymphal immune status affected harp size only, with LPS-males having smaller harps than control-injected males. In addition, the harps of LPS-males showed a lesser degree of melanization, indicating an enhanced substrate use by the melanin-producing enzyme cascade of the immune system. Thus, past immune status is specifically mirrored in sexual traits, suggesting a key role for deployment costs of immunity in parasite-mediated sexual selection.     

POSITIVE GENETIC CORRELATION BETWEEN PARASITE RESISTANCE AND BODY SIZE IN A FREE-LIVING UNGULATE POPULATION

Abstract Parasite resistance and body size are subject to directional natural selection in a population of feral Soay sheep (Ovis aries) on the island of St. Kilda, Scotland. Classical evolutionary theory predicts that directional selection should erode additive genetic variation and favor the maintenance of alleles that have negative pleiotropic effects on other traits associated with fitness. Contrary to these predictions, in this study we show that there is considerable additive genetic variation for both parasite resistance, measured as fecal egg count (FEC), and body size, measured as weight and hindleg length, and that there are positive genetic correlations between parasite resistance and body size in both sexes. Body size traits had higher heritabilities than parasite resistance. This was not due to low levels of additive genetic variation for parasite resistance, but was a consequence of high levels of residual variance in FEC. Measured as coefficients of variation, levels of additive genetic variation for FEC were actually higher than for weight or hindleg length. High levels of additive genetic variation for parasite resistance may be maintained by a number of mechanisms including high mutational input, balancing selection, antagonistic pleiotropy, and host‐parasite coevolution. The positive genetic correlation between parasite resistance and body size, a trait also subject to sexual selection in males, suggests that parasite resistance and growth are not traded off in Soay sheep, but rather that genetically resistant individuals also experience superior growth.     

Anatomy of a cline: dissecting anti‐predatory adaptations in a marine gastropod along the U.S. Atlantic coast

The scope of anti‐predatory adaptation is expected to be greater in warm than in cold environments. High temperatures lower the costs associated with the production and maintenance of energetically expensive traits and enable ecological interactions to intensify. We tested this hypothesis by characterizing the expression of anti‐predatory morphology within a marine gastropod species (the knobbed whelk Busycon carica) over a large (> 1400 km) geographic area that spans more than 10°C annual temperature variation. We also conducted experimental predation studies with a powerful durophagous predator, the stone crab Menippe, to verify the anti‐predatory advantages of a heavily ornamented shell morphology (e.g. increased thickness, pronounced spines), and we used repair scar data to assess clinal variation in selective pressure from predators. We predicted that repair scar rates would be greatest in warm southernmost latitudes, and that expression of energetically costly anti‐predatory morphology would peak in concert with elevated predation pressures. Experiments confirmed that whelks with energetically costly, heavily ornamented shells had higher survivorship rates than those with weakly ornamented shells. As predicted, we also found that the expression of anti‐predatory traits was greatest in the southern part of B. carica's range. After standardizing shells for size, shape, and exposure time to enemies, repair scar rates also peaked to the south. Taken together, these results suggest that the expression of anti‐predatory traits along the geographic cline is governed by the interaction of two selective factors: temperature and predation, with the former acting as the ultimate control on the scope of adaptation both by escalating predation pressure in the southern part of B. carica's range and by physically limiting (to the north) and facilitating (to the south) the production of anti‐predatory traits. Feedbacks between temperature and predation thus causally interact to enable and drive, respectively, the observed geographic cline in energy‐intensive anti‐predatory shell traits.     

Morphological Adaptations to Migration in Birds

Migratory flight performance has direct or carry-over effects on fitness. Therefore, selection is expected to act on minimizing the costs of migratory flight, which increases with the distance covered. Aerodynamic theory predicts how morphological adaptations improve flight performance. These predictions have rarely been tested in comparative analyses that account for scaling and phylogenetic effects. We amassed a unique dataset of 149 European bird species and 10 morphological traits. Mass-adjusted aspect ratio increased, while mass-adjusted heart weight and wing loading decreased with increasing migration distance. These results were robust to whether the analyses were based on the entire species pool or limited to passerines or migrants. Our findings indicate that selection due to migration acts on wing traits that reduce the energetic cost of transportation to increase the flight range. Consequently, the demands for high ‘exercise organ’ performance might be low, and hence such energetically expensive tissues are not associated (pectoral muscle) or are inversely associated (heart) with migration distance.     

Fitness costs of herbicide resistance across natural populations of the common morning glory,Ipomoea purpurea

Although fitness costs associated with plant defensive traits are widely expected, they are not universally detected, calling into question their generality. Here, we examine the potential for life‐history trade‐offs associated with herbicide resistance by examining seed germination, root growth, and above‐ground growth across 43 naturally occurring populations of Ipomoea purpurea that vary in their resistance to RoundUp ® , the most commonly used herbicide worldwide. We find evidence for life‐history trade‐offs associated with all three traits; highly resistant populations had lower germination, shorter roots, and smaller above‐ground size. A visual exploration of the data indicated that the type of trade‐off may differ among populations. Our results demonstrate that costs of adaptation may be present at stages other than simply the production of progeny in this agricultural weed. Additionally, the cumulative effect of costs at multiple life cycle stages can result in severe consequences to fitness when adapting to novel environments.     

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.     

Male mealworm beetles increase resting metabolic rate under terminal investment

Harmful parasite infestation can cause energetically costly behavioural and immunological responses, with the potential to reduce host fitness and survival. It has been hypothesized that the energetic costs of infection cause resting metabolic rate (RMR) to increase. Furthermore, under terminal investment theory, individuals exposed to pathogens should allocate resources to current reproduction when life expectancy is reduced, instead of concentrating resources on an immune defence. In this study, we activated the immune system of Tenebrio molitor males via insertion of nylon monofilament, conducted female preference tests to estimate attractiveness of male odours and assessed RMR and mortality. We found that attractiveness of males coincided with significant down‐regulation of their encapsulation response against a parasite‐like intruder. Activation of the immune system increased RMR only in males with heightened odour attractiveness and that later suffered higher mortality rates. The results suggest a link between high RMR and mortality and support terminal investment theory in T. molitor.     

Costs of parasite resistance for female survival and parental care in a freshwater isopod

Parasite resistance is expected to be costly because activation and maintenance of immune system requires energy that will not be available for other fitness related functions. Here, we experimentally exposed gravid female isopods from two lake populations to trophically transmitted acanthocephalan parasite. Successful establishment of the parasite requires penetration to body cavity; therefore, it is likely to induce an immune response. Resistant females from a lake where the parasite occurs as well as from a lake without the parasite experienced higher mortality than susceptible or control females. Parasite exposure reduced the offspring size at birth in both susceptible, but especially, in resistant females, suggesting that resistant females had less resource to direct for parental care. Parasite exposure had no effect on brood dumping, time to release of offspring or offspring growth rate after birth. Hence, our results reveal costs of resistance in parental survival and parental care of offspring.